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Long-term trends in intrinsic water-use efficiency and growth of subtropical Pinus tabulaeformis Carr. and Pinus taiwanensis Hayata in central China

  • SOILS, SEC 2 • GLOBAL CHANGE, ENVIRON RISK ASSESS, SUSTAINABLE LAND USE • RESEARCH ARTICLE
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Abstract

Purpose

This study analysed tree-ring stable carbon isotope composition (δ13C) of Pinus tabulaeformis Carr. and Pinus taiwanensis Hayata, from a subtropical forest located in central China for the last 130 years, to obtain the long-term trends of δ13C, carbon isotope discrimination by plants (Δ), leaf internal carbon dioxide (CO2) concentration (c i ) and intrinsic water-use efficiency (iWUE) in response to elevated atmospheric CO2 concentration (c a ) and climate change and explore how environmental changes affected long-term tree physiological responses and growth.

Materials and methods

Tree-ring cores were taken in Dabie Mountains, the border of Hubei, Henan and Anhui Provinces of China. δ13C was undertaken at every 3-year interval, and Δ, c i , iWUE and basal area increment (BAI) were determined. Regression analysis was used to quantify the trends in climate and the relationships of c i , iWUE and BAI with elevated c a and climate. Partial correlation analysis was used to distinguish the effects of c a and climate on c i and iWUE.

Results and discussion

δ13C of P. tabulaeformis and P. taiwanensis decreased in the past 130 years, but Δ had no obvious change over time for the two tree species. Both c i and iWUE increased significantly with the calendar year. BAI of P. tabulaeformis continuously increased during 1897–1993, but decreased slightly in the recent 20 years. However, BAI of P. taiwanensis did not present obvious change in the period 1882–2010. The c i and iWUE of P. tabulaeformis and P. taiwanensis also increased linearly with elevated c a in the past 130 years and with mean annual temperature during 1960–2007. Partial correlation analysis showed that elevated c a , not temperature, induced the changes in c a and iWUE. BAI of P. tabulaeformis since 1897 and that of P. taiwanensis during 1975–2010 responded quadratically to elevated c a . Warming-deduced drought in the study area in the recent 30 years resulted in increases in iWUE and decreases in BAI.

Conclusions

This study showed that while iWUE increased in the past 130 years, tree growth of two subtropical tree species in central China responded to rising c a non-linearly. Negative effects of some factors on tree growth, such as climate change (particularly warming-induced drought), nutrient limitation and physiological long-term acclimation to elevated c a , have overridden the CO2 fertilization effects in the past 30 years.

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References

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol 165:351–371

    Article  Google Scholar 

  • Allen MR, Frame DJ, Huntingford C, Jones CD, Lowe JA, Meinshausen M, Meinshausen N (2009) Warming caused by cumulative carbon emissions towards the trillionth tonne. Nature 458:1163–1166

    Article  CAS  Google Scholar 

  • Andreu-Hayles L, Planells O, Gutierrez E, Muntan E, Helle G, Anchukaitis KJ, Schleser GH (2011) Long tree-ring chronologies reveal 20th century increases in water-use efficiency but no enhancement of tree growth at five Iberian pine forests. Glob Change Biol 17:2095–2112

    Article  Google Scholar 

  • Arneth A, Lloyd J, Santruckova H, Bird M, Grigoryev S, Kalaschnikov YN, Gleixner G, Schulze ED (2002) Response of central siberian scots pine to soil water deficit and long-term trends in atmospheric CO2 concentration. Global Biogeochem Cy 16:5-1–5-13

    Article  Google Scholar 

  • Barber VA, Juday GP, Finney BP (2000) Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. Nature 405:668–673

    Article  CAS  Google Scholar 

  • Battipaglia G, Saurer M, Cherubini P, Calfapietra C, McCarthy HR, Norby RJ, Cotrufo MF (2013) Elevated CO2 increases tree-level intrinsic water use efficiency: insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites. New Phytol 197:544–554

    Article  CAS  Google Scholar 

  • Bert D, Leavitt SW, Dupouey JL (1997) Variations of wood δ13C and water-use efficiency of Abies alba during the last century. Ecology 78:1588–1596

    Google Scholar 

  • Brienen RJW, Wanek W, Hietz P (2011) Stable carbon isotopes in tree rings indicate improved water use efficiency and drought responses of a tropical dry forest tree species. Trees-struct Funct 25:103–113

    Article  CAS  Google Scholar 

  • Duquesnay A, Bréda N, Stievenard M, Dupouey JL (1998) Changes of tree-ring δ13C and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell Environ 21:565–572

    Article  Google Scholar 

  • Ehleringer JR, Cerling TE (1995) Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants. Tree Physiol 15:105–111

    Article  Google Scholar 

  • Etheridge DM, Steele LP, Langenfelds RL, Francey RJ, Barnola JM, Morgan VI (1996) Natural and anthropogenic changes in atmospheric CO2 over the last 1000 years from air in Antarctic ice and firn. J Geophys Res 101:4115–4128

    Article  CAS  Google Scholar 

  • Etheridge DM, Steele LP, Francey RJ, Langenfelds RL (1998) Atmospheric methane between 1000 A.D. and present: evidence of anthropogenic emissions and climatic variability. J Geophys Res 103:15979–15993

    Article  CAS  Google Scholar 

  • Farquhar GD, Oleary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the inter-cellular carbon-dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    Article  CAS  Google Scholar 

  • Feng XH (1999) Trends in intrinsic water-use efficiency of natural trees for the past 100–200 years: a response to atmospheric CO2 concentration. Geochim Cosmochim Ac 63:1891–1903

    Article  CAS  Google Scholar 

  • Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31

    Article  CAS  Google Scholar 

  • Gagen M, McCarroll D, Robertson I, Loader NJ, Jalkanen R (2008) Do tree ring δ13C series from Pinus sylvestris in northern Fennoscandia contain long-term non-climatic trends? Chem Geol 252:42–51

    Article  CAS  Google Scholar 

  • Gomez-Guerrero A, Silva LCR, Barrera-Reyes M, Kishchuk B, Velazquez-Martinez A, Martinez-Trinidad T, Ofelia Plascencia-Escalante F, Horwath WR (2013) Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests. Glob Change Biol 19:1748–1758

    Article  Google Scholar 

  • Hietz P, Wanek W, Dunisch O (2005) Long-term trends in cellulose δ13C and water-use efficiency of tropical Cedrela and Swietenia from Brazil. Tree Physiol 25:745–752

    Article  CAS  Google Scholar 

  • Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bull 43:69–78

    Google Scholar 

  • Ivlev A, Voronin VV (2007) The mechanism of carbon isotope fractionation in photosynthesis and carbon dioxide component of the greenhouse effect. Biol Bull 34:603–609

    Article  CAS  Google Scholar 

  • Kirdyanov AV, Treydte KS, Nikolaev A, Helle G, Schleser GH (2008) Climate signals in tree-ring width, density and δ13C from larches in Eastern Siberia (Russia). Chem Geol 252:31–41

    Article  CAS  Google Scholar 

  • Kӧrner C (2009) Responses of humid tropical trees to rising CO2. Annu Rev Ecol Evol Syst 40:61–79

    Article  Google Scholar 

  • Lacis AA, Schmidt GA, Rind D, Ruedy RA (2010) Atmospheric CO2: principal control knob governing earth’s temperature. Science 330:356–359

    Article  CAS  Google Scholar 

  • LaMarche VC, Graybill DA, Fritts HC, Rose MR (1984) Increasing atmospheric carbon dioxide: tree ring evidence for growth enhancement in natural vegetation. Science 225:1019–1021

    Article  Google Scholar 

  • Leavitt SW, Idso SB, Kimball BA, Burns JM, Sinha A, Stott L (2003) The effect of long-term atmospheric CO2 enrichment on the intrinsic water-use efficiency of sour orange trees. Chemosphere 50:217–222

    Article  CAS  Google Scholar 

  • LeBlanc DC (1990) Relationships between breast-height and whole-stem growth indexes for red spruce on Whiteface Mountain, New York. Can J Forest Res 20:1399–1407

    Article  Google Scholar 

  • Linares JC, Camarero JJ (2012) From pattern to process: linking intrinsic water-use efficiency to drought-induced forest decline. Glob Change Biol 18:1000–1015

    Article  Google Scholar 

  • Linares JC, Delgado-Huertas A, Camarero JJ, Merino J, Carreira JA (2009) Competition and drought limit the response of water-use efficiency to rising atmospheric carbon dioxide in the Mediterranean fir Abies pinsapo. Oecologia 161:611–624

    Article  Google Scholar 

  • Liu XH, Shao XM, Liang EY, Zhao LJ, Chen T, Qin D, Ren JW (2007) Species-dependent responses of juniper and spruce to increasing CO2 concentration and to climate in semi-arid and arid areas of northwestern China. Plant Ecol 193:195–209

    Article  Google Scholar 

  • Liu XH, Shao XM, Wang LL, Liang E, Qin DH, Ren JW (2008) Response and dendroclimatic implications of δ13C in tree rings to increasing drought on the northeastern Tibetan Plateau. J Geophys Res 113:doi:10.1029/2007JG000610

  • Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    Article  CAS  Google Scholar 

  • MacFarling MC (2004) The natural and anthropogenic variations of carbon dioxide, methane and nitrous oxide during the Holocene from ice core analysis. PhD thesis, University of Melbourne, Melbourne, Australia

  • MacFarling MC, Etheridge D, Trudinger C, Steele P, Langenfelds R, van Ommen T, Smith A, Elkins J (2006) Law dome CO2, CH4 and N2O ice core records extended to 2000 years BP. Geophys Res Lett 33: doi: 10.1029/2006GL026152

  • Mann ME, Bradley RS, Hughes MK (1998) Global-scale temperature patterns and climate forcing over the past six centuries. Nature 392:779–787

    Article  CAS  Google Scholar 

  • Maseyk K, Hemming D, Angert A, Leavitt SW, Yakir D (2011) Increase in water-use efficiency and underlying processes in pine forests across a precipitation gradient in the dry Mediterranean region over the past 30 years. Oecologia 167:573–585

    Article  Google Scholar 

  • Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomaki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264

    Article  Google Scholar 

  • Montzka SA, Dlugokencky EJ, Butler JH (2011) Non-CO2 greenhouse gases and climate change. Nature 476:43–50

    Article  CAS  Google Scholar 

  • Morison JIL (1993) Response of plants to CO2 under water limited conditions. Vegetatio 104:193–209

    Article  Google Scholar 

  • Morsion JIL (1987) Intercellular CO2 concentration and stomatal response to CO2. In: Zeiger E, Farquhar GD, GCowan IR (eds) Stomatal function. Stanford University Press, Stanford, CA, USA, pp 229–251

    Google Scholar 

  • Nock CA, Baker PJ, Wanek W, Leis A, Grabner M, Bunyavejchewin S, Hietz P (2011) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Glob Change Biol 17:1049–1063

    Article  Google Scholar 

  • Ou TH, Qian WH (2006) Vegetation variations along the monsoon boundary zone in East Asia. Chinese J Geophys-ch 49:698–705

    Article  Google Scholar 

  • Overdieck D, Forstreuter M (1994) Evapotranspiration of beech stands and transpiration of beech leaves subject to atmospheric CO2 enrichment. Tree Physiol 14:997–1003

    Article  Google Scholar 

  • Pedersen BS (1998) The role of stress in the mortality of midwestern oaks as indicated by growth prior to death. Ecology 79:79–93

    Article  Google Scholar 

  • Peñuelas J, Hunt JM, Ogaya R, Jump AS (2008) Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Glob Change Biol 14:1076–1088

    Article  Google Scholar 

  • Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Global Ecol Biogeogr 20:597–608

    Article  Google Scholar 

  • Phipps RL, Whiton JC (1988) Decline in long-term growth trends of white oak. Can J Forest Res 18:24–32

    Article  Google Scholar 

  • Picon C, Guehl JM, Aussenac G (1996) Growth dynamics, transpiration and water-use efficiency in Quercus robur plants submitted to elevated CO2 and drought. Ann Des Sci For 53:431–446

    Article  Google Scholar 

  • Saurer M, Cherubini P, Bonani G, Siegwolf R (2003) Tracing carbon uptake from a natural CO2 spring into tree rings: an isotope approach. Tree Physiol 23:997–1004

    Article  CAS  Google Scholar 

  • Saurer M, Siegwolf RTW, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Glob Change Biol 10:2109–2120

    Article  Google Scholar 

  • Sidorova OV, Siegwolf RTW, Saurer M, Naurzbaev MM, Vaganov EA (2008) Isotopic composition (δ13C, δ18O) in wood and cellulose of Siberian larch trees for early medieval and recent periods. J Geophys Res 113:doi:10.1029/2007JG000473

  • Silva LCR, Anand M (2013) Probing for the influence of atomospheric CO2 and climate change on forest ecosystems across biomes. Glob Change Biol 22:83–92

    Google Scholar 

  • Silva LCR, Anand M, Oliveira JM, Pillar VD (2009) Past century changes in Araucaria angustifolia (Bertol.) Kuntze water use efficiency and growth in forest and grassland ecosystems of southern Brazil: implications for forest expansion. Glob Change Biol 15:2387–2396

    Article  Google Scholar 

  • Silva LCR, Anand M, Leithead MD (2010) Recent widespread tree growth decline despite increasing atmospheric CO2. PLoS One 5: doi:10.1371/journal.pone.0011543

  • Silva LCR, Horwath WR (2013) Explaining global increases in water use efficiency: why have we overestimated responses to rising atmospheric CO2 in natural forest ecosystems? PLoS One 8: doi:10.1371/journal.pone.0053089

  • Stokes MA, Smiley TL (1968) An introduction to tree-ring dating. An introduction to tree-ring dating. University of Chicago Press, Chicago

    Google Scholar 

  • Sun FF, Kuang YW, Wen DZ, Xu ZH, Li JL, Zuo WD, Hou EQ (2010) Long-term tree growth rate, water use efficiency, and tree ring nitrogen isotope composition of Pinus massoniana L. in response to global climate change and local nitrogen deposition in Southern China. J Soils Sediments 10:1453–1465

    Article  CAS  Google Scholar 

  • Tang KL, Feng XH, Funkhouser G (1999) The δ13C of tree rings in full-bark and strip-bark bristlecone pine trees in the white mountains of California. Glob Change Biol 5:33–40

    Article  Google Scholar 

  • Wang W, Liu X, An W, Xu G, Zeng X (2012) Increased intrinsic water-use efficiency during a period with persistent decreased tree radial growth in northwestern China: causes and implications. Forest Ecol Manag 275:14–22

    Article  Google Scholar 

  • Waterhouse JS, Switsur VR, Barker AC, Carter AHC, Hemming DL, Loader NJ, Robertson I (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quaternary Sci Rev 23:803–810

    Article  Google Scholar 

  • Whitmore TC (1990) An introduction to tropical rainforests. Oxford University, Oxford, UK

    Google Scholar 

  • Wullschleger SD, Tschaplinski TJ, Norby RJ (2002) Plant water relations at elevated CO2—implications for water-limited environments. Plant Cell Environ 25:319–331

    Article  Google Scholar 

  • Xu G, Liu X, Qin D, Chen T, An W, Wang W, Wu G, Zeng X, Ren J (2013) Climate warming and increasing atmospheric CO2 have contributed to increased intrinsic water-use efficiency on the northeastern Tibetan Plateau since 1850. Trees-struct Funct 27:465–475

    Article  Google Scholar 

  • Xu ZH, Chen CR, He JZ, Liu JX (2009) Trends and challenges in soil research 2009: linking global climate change to local long-term forest productivity. J Soils Sediments 9:83–88

    Article  Google Scholar 

  • Xu ZH, Saffigna PG, Farquhar GD, Simpson JA, Haines RJ, Walker S, Osborne DO, Guinto D (2000) Carbon isotope discrimination and oxygen isotope composition in clones of the F1 hybrid between slash pine and Caribbean pine in relation to tree growth, water-use efficiency and foliar nutrient concentration. Tree Physiol 20:1209–1217

    Article  CAS  Google Scholar 

  • Yamaguchi DK (1991) A simple method for cross-dating increment cores from living trees. Can J Forest Res 21:414–416

    Article  Google Scholar 

  • Zeppel MJB, Lewis JD, Chaszar B, Smith RA, Medlyn BE, Huxman TE, Tissue DT (2012) Nocturnal stomatal conductance responses to rising [CO2], temperature and drought. New Phytol 193:929–938

    Article  CAS  Google Scholar 

  • Zheng Y, Zhang Y, Shao X, Yin Z-Y, Zhang J (2012a) Temperature variability inferred from tree-ring widths in the Dabie Mountains of subtropical central China. Trees-struct Funct 26:1887–1894

    Article  Google Scholar 

  • Zheng Y, Zhang Y, Shao X, Yin Z-Y, Zhang J (2012b) Climate significance of tree ring width of Huangshan pine and Chinese pine in the Dabie Mountains. Prog Geography 31:72–77 (in Chinese with English abstract)

    CAS  Google Scholar 

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Acknowledgments

This research was supported by the Australian Research Council (DP1092470), Griffith University (Australia). We thank Prof. Zhi-Yong Yin, Dr. Yonghong Zheng and Dr. Yong Zhang for their assistance in the field work and Mr Rene Diocares for his assistance in stable isotope analyses.

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Authors and Affiliations

  1. Environmental Futures Centre and School of Biomolecular and Physical Sciences, Griffith University, Nathan, Brisbane, Queensland, 4111, Australia

    Yan Xu, Zhihong Xu & Putranto Nugroho

  2. Environmental Futures Centre, Griffith University, Nathan, Queensland, 4111, Australia

    Wenjing Li

  3. Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Xuemei Shao

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  1. Yan Xu
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  2. Wenjing Li
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  3. Xuemei Shao
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Correspondence to Zhihong Xu.

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Responsible editor: Hailong Wang

Yan Xu and Wenjing Li contributed equally to this work.

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Xu, Y., Li, W., Shao, X. et al. Long-term trends in intrinsic water-use efficiency and growth of subtropical Pinus tabulaeformis Carr. and Pinus taiwanensis Hayata in central China. J Soils Sediments 14, 917–927 (2014). https://doi.org/10.1007/s11368-014-0878-4

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